A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females

Summary

Female fruit flies change their food preferences after mating, becoming attracted to nutrients important for egg production. This study reveals that during mating, pheromone detection triggers dopamine-driven changes in the fly’s brain learning center. These neural changes essentially ‘remember’ mating experience and reprogram the female’s sense of smell, even though the sensory neurons return to normal within hours. This demonstrates how an animal can learn from mating experience to make better nutritional choices as a mother.

Background

Reproductive state induces dramatic shifts in female chemosensory perception and preferences. Previous research showed that mating induces a transient neuropeptidergic modulation of olfactory sensory neurons in Drosophila females, leading to increased preference for polyamines. However, this sensory modulation declines within hours while the behavioral change persists for days, suggesting higher brain involvement.

Objective

To investigate the neural circuits and mechanisms underlying mating-induced long-lasting changes in female odor perception and preference for polyamines, particularly the role of the mushroom body and dopaminergic neurons in reproductive state-dependent behavior.

Results

Mating-related olfactory signals, particularly pheromone detection via ORCO, are required during mating to induce lasting polyamine preference. Mushroom body Kenyon cells are necessary during mating and test for preference expression. Dopaminergic neurons innervating the β’1 compartment can replace mating experience, while specific mushroom body output neurons modulate preference behavior bidirectionally depending on reproductive state.

Conclusion

A dopamine-gated learning circuit in the mushroom body underpins how mating experience lastingly alters female odor perception through sensory experience at the time of mating, integrating pheromone signals to modulate preference for nutritionally important polyamines.
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